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Jeon BC, Kim YJ, Park AK, Song MR, Na KM, Lee J, An D, Park Y, Hwang H, Kim TD, Lim J, Park SK. Dynamic O-GlcNAcylation governs long-range chromatin interactions in V(D)J recombination during early B-cell development. Cellular & molecular immunology 2025 22(1) 39627609
Abstract:
V(D)J recombination secures the production of functional immunoglobulin (Ig) genes and antibody diversity during the early stages of B-cell development through long-distance interactions mediated by cis-regulatory elements and trans-acting factors. O-GlcNAcylation is a dynamic and reversible posttranslational modification of nuclear and cytoplasmic proteins that regulates various protein functions, including DNA-binding affinity and protein-protein interactions. However, the effects of O-GlcNAcylation on proteins involved in V(D)J recombination remain largely unknown. To elucidate this relationship, we downregulated O-GlcNAcylation in a mouse model by administering an O-GlcNAc inhibitor or restricting the consumption of a regular diet. Interestingly, the inhibition of O-GlcNAcylation in mice severely impaired Ig heavy-chain (IgH) gene rearrangement. We identified several factors crucial for V(D)J recombination, including YY1, CTCF, SMC1, and SMC3, as direct targets of O-GlcNAc modification. Importantly, O-GlcNAcylation regulates the physical interaction between SMC1 and SMC3 and the DNA-binding patterns of YY1 at the IgH gene locus. Moreover, O-GlcNAc inhibition downregulated DDX5 protein expression, affecting the functional association of CTCF with its DNA-binding sites at the IgH locus. Our results showed that locus contraction and long-range interactions throughout the IgH locus are disrupted in a manner dependent on the cellular O-GlcNAc level. In this study, we established that V(D)J recombination relies on the O-GlcNAc status of stage-specific proteins during early B-cell development and identified O-GlcNAc-dependent mechanisms as new regulatory components for the development of a diverse antibody repertoire.
O-GlcNAc proteins:
MPEG1, CUL4B, DHX8, RHG27, VIR, PNISR, FRPD1, RENT2, LAS1L, ITIH4, THOC2, MMRN1, PYR1, YTDC2, PTPRB, ANR44, RBM25, OSBL8, DAAF5, SAFB1, KI67, DESP, YTDC1, UBE4A, NUMA1, MORC3, HXK2, LEG9, KNG1, UBE3A, DCTN1, DIAP1, U5S1, RL21, PHB2, CPSF2, DHX15, EXOC4, STAG2, AP1B1, PININ, HNRH1, SP100, GP1BA, ITB3, RL35A, SPT5H, DHX9, E41L2, BAZ1A, ZFR, ROA2, PRS6A, FA5, AFAM, COR1A, SP1, C1QR1, COX2, AMY1, CO3, CO4B, B2MG, HBA, HBB1, K1C10, K2C1, CFAB, ALDOA, TBA1B, TBA3, ITAM, K1C18, LDHA, LCK, APOA4, PTPRC, CFAH, TTHY, ANXA2, ALBU, A1AT1, SPA3K, HS90A, TRFL, ENPL, APOE, MDHM, GNAI2, RPB1, ITB1, PDIA1, NUCL, APOA2, PTPRQ, CALM2, EF1A1, 4F2, PARP1, PERM, FINC, HS90B, K2C8, ITA5, ITB2, TCPA, RL7A, GELS, ICAM1, DNMT1, S10A6, RL27A, RS16, RL7, RSSA, LMNB1, ANXA6, RLA0, CD44, LEUK, H12, CN37, AMPE, HS71L, G3P, LAMP2, HSP72, ENOA, PTBP1, PPIA, TPIS, LYZ1, PCNA, PTPRA, BASI, KS6A1, KS6A3, COF1, FAS, THRB, RL13A, BIP, VIME, PLMN, VTDB, A1AT2, CBL, AP1G1, EIF3A, EST1C, ITAL, CD11B, MCM3, RS2, CD19, UBF1, TLN1, EZRI, MOES, KLKB1, H2AX, VAV, NCKP1, MUG1, KIF2A, DPP4, PTN6, FETUA, C5AR1, CEAM1, CD68, ANT3, SYWC, KIF4, DPOLA, RAB5C, RAB18, CD22, TSP1, CALX, RFC1, PRDX1, RL12, RL18, DNLI1, GRP75, DYN2, RL28, MMP9, STAT1, STA5B, EPS15, TCPQ, MSH2, H14, H15, RAGP1, SIPA1, NSF, PRS7, BRCC3, NEDD4, CAPZB, RL6, RL5, RL13, RL36, KSYK, PERE, ROA1, MCM4, MCM5, SAHH, K2C6A, VATA, PA2G4, RAB7A, RL9, ADT2, IMA1, PON1, DPOD1, UBP10, KPYM, STAT6, RL10A, CEBPZ, PIPNB, MSH6, UBP5, ATPB, UBP25, NICA, ACTN4, EF2, OPA1, FOXP1, TPM2, WDHD1, ARPC4, RUVB1, PCBP1, ACTB, IF4A1, RS20, UB2D3, ARF3, RL26, RL27, RL37A, ARF4, HNRPK, RS7, PRS4, RS8, RS15A, RS14, RS23, RS18, RS11, RS13, SMD2, ARF6, PRS10, RS4X, RL18A, RL23A, RS6, H4, VATB2, RAB1A, RAN, RL23, RS24, RS25, RS26, RL30, RL31, RS3, RL8, PROF1, RL40, HSP7C, PHB1, RL22, RACK1, ACTS, TBA4A, TBB4B, 1433F, IMB1, M4K1, PKN1, STIM1, PYRG2, ROCK1, RAD50, PYRG1, TCPH, TCPB, TCPD, TCPE, TCPZ, TCPG, WNK1, RHOG, RL19, H33, BACH2, MCM2, MCM6, RS3A, ANX11, SMRC1, FUMH, ARVC, TBB5, APOA1, A1AT4, TYY1, HNRL2, LYAM3, TOP2A, APOH, TERA, UBA1, PLAK, ATPA, IKZF1, SPA3M, SMRCD, TOP1, RAC2, PYC, IF2P, CBG, ACADS, AMBP, PECA1, SSRP1, ZCH18, K2C80, PSA, PTCD3, NSUN2, EDEM3, MCM9, TMC5, HMHA1, HP1B3, GUAA, H2AV, SMCA4, PRC2C, MIDN, K1C26, K22E, PSMD1, BRE1B, ESYT1, AAK1, RHG17, EDC4, UBP19, GPD1L, ELNE, SC31A, IQGA2, K22O, ITB2L, C1TM, UN13A, PLCH1, PDS5B, CENPJ, DDX46, TR150, A16A1, EHMT1, MCTP2, RBM27, CYFP2, PSME4, MYO1G, LC7L3, PUR4, MYH1, LEO1, SIN3A, XRCC1, ODO1, HNRPD, SAMH1, HELLS, ARHG2, I17RA, PML, 2A5G, PPM1G, CFAI, CERU, CTCF, PRDX2, EZH2, HCFC1, PA1B3, ARHG1, PLSL, A2AP, HSP74, DSG1A, GSLG1, EWS, RAD21, FSCN1, GDIB, DDX5, HS105, ITIH2, ITA6, EI2BD, SERA, KINH, PDCD4, PZP, PRG2, MYH10, MCM7, NPM, PCBP2, CTR9, DDX3X, CD180, SPTB2, SPR1A, TIF1B, TFR1, RU17, SPT6H, NDUA4, IF4G2, MINT, RHG30, H2B1B, TOP2B, TPP2, AT2A3, H2A2C, VINC, PUR2, CLH1, SYMC, GNPTA, PDS5A, CDC5L, CE290, F120A, UBP7, JADE3, K1C42, K2C72, SR140, K2C73, S23IP, IF4G1, RBM26, P4R3A, U520, ABCF1, SMHD1, UGGG1, XPO1, ANO6, KIF15, KIF11, FHOD1, FKB15, PTN23, LPPRC, SMRC2, ECM29, CHD4, PK3C3, NUP98, GMIP, NFRKB, TEX2, UBE2O, KDM3B, CE162, CNOT1, CAND1, LARP1, VIP2, RS9, RL35, RS27L, 2AAA, SND1, ASAP2, IPO8, HUWE1, LC7L2, MBB1A, INT7, CTDP1, PP6R1, ELP1, DCAF1, CLAP1, SCRIB, PUM1, NU214, NAA15, FACD2, FBLL1, UBP2L, SYMPK, SIG10, DDX42, ANFY1, EFTU, TNPO1, ROA3, PLD4, SYAC, S2512, NU107, PTBP3, NRDC, ERC6L, GANAB, SP130, NUP93, SUN2, RCC2, IPO5, EMSY, ODP2, RBGPR, SYLC, SYQ, ECHA, RL24, CLAP2, CNDH2, PB1, FLNA, SYIC, IFIX, CIP2A, GEMI5, UBP47, CTL2, TBCD, POGZ, ANC2, KS6A5, EFL1, LCAP, DOCK8, CND2, IWS1, RBM14, DOCK2, UBA6, MIC60, UFL1, VCIP1, NUP88, NED4L, RPB2, AQR, SMC4, SMC2, SYEP, TCRG1, LONM, OGT1, CHERP, CCAR1, INT5, PYGB, COPA, PLCG2, INT4, EIF3B, BCLF1, K319L, URP2, DNM1L, NEK9, FCHO1, PAF1, IPO11, CND1, MATR3, PLCL2, DP13A, PO121, SF3A1, HNRPL, NU133, EIF3C, BST2, CD177, ADIPL, CDC16, STPAP, LRC8C, ACSF2, EVI2B, MYH9, UHRF1, VIGLN, ADPGK, PSMD2, HNRL1, AT1A1, MICA1, CCAR2, DX39A, SRSF4, K2C79, RFA1, HNRPU, S25A3, RBM39, SEC63, IPO4, SFPQ, ACLY, IF4A3, NDUS1, ATPG, DDX1, UBAP2, HEMO, IPO9, RBM5, PRP6, SMCA5, SP16H, TADBP, SF3B3, SYDC, PP6R3, C1TC, NOP2, PDE2A, KIF2C, K2C5, SIR1, XPO5, SMRD2, ECHB, ARP3, EMIL1, UN45A, ACON, DPP3, HSP7E, GTPB4, ARBK1, SRRT, SF3B1, NU155, RRBP1, DHX30, RL17, NUDC2, 6PGL, COTL1, RM18, TRAP1, AT5F1, RL14, XPOT, PRPS2, RRP44, SMC1A, SMUF1, SMC3, PUR9, SNX2, ROA0, RL11, GARS, RL15, MTREX, MMS19, HNRPM, SYRC, NH2L1, RL34, GRIFN, UB2V2, S10AE, CORO7, STAG1, CUL5, SC23B, CALL3, NOP56, RL4, EF1G, PRP4, QCR2, PELP1, AP2B1, XRN2, NVL, EIF3K, 6PGD, SYF1, EIF3F, XPO7, IPO7, RENT1, BCAP, PESC, ERAP1, VPS35, EHD4, TFP11, XPO2, PKHA2, RBP2, UBE4B, SHIP1, HRG, XPO4, AN32B, GTF2I, DYHC1, STK4, COPB, DDX21, ACINU, FLII, IQGA1, HYOU1, HIP1R, FMNL1, SACS, SART3, GIT2, MY18A, ITA2B, FAK2, CAF1A, K1C17, FETUB, PLEC, PO210, ADDA, PCLO, COPG1, UBQL2, H2AY, ZEB2, GALK1, SC11A, MTA2, PR40A, TIM, MYO1C, INSRR, MD1L1, PDC6I, PFKAP, CXA10, GANP, IF2G, ADNP, P5CS, SAE2, ARI1, DX39B, CLIC1, SYVC, AP3B1, ILF3, USO1, HNRPC, BAZ1B, K1C16, SNUT1
Species: Mus musculus
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Zhu WZ, Palazzo T, Zhou M, Ledee D, Olson HM, Paša-Tolić L, Olson AK. First comprehensive identification of cardiac proteins with putative increased O-GlcNAc levels during pressure overload hypertrophy. PloS one 2022 17(10) 36288343
Abstract:
Protein posttranslational modifications (PTMs) by O-GlcNAc globally rise during pressure-overload hypertrophy (POH). However, a major knowledge gap exists on the specific proteins undergoing changes in O-GlcNAc levels during POH primarily because this PTM is low abundance and easily lost during standard mass spectrometry (MS) conditions used for protein identification. Methodologies have emerged to enrich samples for O-GlcNAcylated proteins prior to MS analysis. Accordingly, our goal was to identify the specific proteins undergoing changes in O-GlcNAc levels during POH. We used C57/Bl6 mice subjected to Sham or transverse aortic constriction (TAC) to create POH. From the hearts, we labelled the O-GlcNAc moiety with tetramethylrhodamine azide (TAMRA) before sample enrichment by TAMRA immunoprecipitation (IP). We used LC-MS/MS to identify and quantify the captured putative O-GlcNAcylated proteins. We identified a total of 700 putative O-GlcNAcylated proteins in Sham and POH. Two hundred thirty-three of these proteins had significantly increased enrichment in POH over Sham suggesting higher O-GlcNAc levels whereas no proteins were significantly decreased by POH. We examined two MS identified metabolic enzymes, CPT1B and the PDH complex, to validate by immunoprecipitation. We corroborated increased O-GlcNAc levels during POH for CPT1B and the PDH complex. Enzyme activity assays suggests higher O-GlcNAcylation increases CPT1 activity and decreases PDH activity during POH. In summary, we generated the first comprehensive list of proteins with putative changes in O-GlcNAc levels during POH. Our results demonstrate the large number of potential proteins and cellular processes affected by O-GlcNAc and serve as a guide for testing specific O-GlcNAc-regulated mechanisms during POH.
O-GlcNAc proteins:
MA7D1, CAVN4, OTUD4, FIBA, TRDN, DPYL2, CLCA, MYH11, KNG1, PRDX6, AKAP1, DLDH, NDUBB, GSTO1, CASQ2, RL21, PHB2, ECH1, NDUA1, TIM44, CAVN1, AKAP2, SLK, NIPS2, AT2A2, PGAM2, EF1B, ATX2, NMT1, XIRP1, PDLI1, MYPC3, SNX3, DC1I2, PLIN4, ROA2, RAD, CLPP, TOM1, COX1, COX2, CAH2, CO3, IGJ, KV2A7, IGKC, GCAB, IGHG1, IGH1M, B2MG, HBA, HBB1, LAMC1, FABP4, CFAB, MYG, ALDOA, ANF, AATC, AATM, TBA1B, LDHA, G6PI, TRY2, TTHY, KCRM, ANXA2, ALBU, SPA3K, ENPL, APOE, MDHM, ITB1, PDIA1, NUCL, PGK1, FRIH, MYL3, SODM, NDUB1, ANXA1, EF1A1, CATB, TAU, THIO, GSTM1, H2B1F, H10, CO1A1, FABPH, HS90B, DMD, PFKAL, COX5A, RL7A, GELS, MYH3, AT1B1, GLUT4, RL7, MDHC, RSSA, CALR, HSPB1, ANXA6, GLNA, B4GT1, GSTM2, H12, LDHB, SPTN1, G3P, ENOA, HXK1, PPIA, TPIS, BASI, COF1, RL13A, SERPH, COX5B, COX41, BIP, PRDX3, VIME, CYTC, ENOB, TGM2, EIF3A, CBX3, CXA1, PIMT, CRYAB, CATA, CAPG, GSTA4, RS2, TLN1, MOES, RADI, CTNA1, DHE3, FKB1A, MAP4, RL3, H2AX, PDIA3, PABP1, FRIL1, FETUA, DESM, AIMP1, LA, ANT3, RANG, MIF, PTN11, HSPB7, ODPA, CALX, PRDX1, RL12, RL18, FBLN2, HMGCL, GRP75, CAP1, TKT, RL28, ACSL1, ECI1, H14, H11, H15, H13, ALDR, COF2, ACADM, PRS7, ADX, ALDH2, CAPZB, RL6, RL29, CACP, RL13, ANXA5, TBCA, LMNA, CX7A2, TNNI3, ADT1, ROA1, PCY1A, CAV1, ODBA, CSRP3, ACADV, PA2G4, TNNT2, ICAL, ACADL, CAV3, MLRV, ADT2, LUM, KPYM, NDUS6, CPT2, RL10A, ODB2, CCHL, MOT1, IDHP, STOM, ADK, ATPK, ACYP2, ATP68, ATP5E, AT5G2, CX6B1, CX7A1, COX7B, CYB5, UBP5, ATPB, WFS1, ACTN4, EF2, OPA1, TPM1, B2L13, PCBP1, ACTB, RS20, PPLA, UB2D3, UBC12, UBE2N, RL26, RL27, SUMO2, 1433G, RS7, RS8, 1433E, RS14, RS18, RS11, RS13, DLRB1, EF1A2, RS4X, RL23A, RS6, H4, RAN, RS15, RS25, RS30, RL30, CYC, RL31, RS3, RL32, RL8, FBX40, YBOX1, RS27A, HSP7C, MPC1, CH60, GNAS2, 1433Z, HMGB1, IF5A1, ACTG, ACTH, RS12, RS10, RL22, ACTC, UB2L3, TBA4A, TBB4B, H31, IMB1, PEBP1, HINT1, IDHG1, NACAM, TCPD, SGCD, SGCA, WNK1, RL19, SRSF3, H32, RS3A, G3BP2, ANXA4, COQ7, G3BP1, LAMA4, QCR6, PRDX5, APOA1, CO1A2, NDKB, TERA, UBA1, MYH6, ATPA, KCRB, CO6A1, PGBM, EMAL1, ATP5I, CLUS, ANXA7, ACADS, CD36, NEBL, PERM1, TRI72, HSDL2, HP1B3, PRC2C, TM38A, Q3TV00, SRSF6, FUBP2, SDHF1, EI3JA, LIMC1, AAK1, NDUB6, MCCB, COBL1, SLMAP, SRBS2, K22O, CPZIP, NDUF2, MYPN, HSPB6, MLIP, IASPP, TM1L2, ODO1, LAMA2, STIP1, REEP5, VDAC2, VDAC1, COQ8A, LAP2B, PRDX2, HCFC1, LAMB2, HSP74, HCDH, FBN1, FXR1, KTN1, GDIB, DDX5, KINH, LASP1, PZP, NPM, NNTM, SNRPA, SPTB2, SPEG, SRBS1, DBNL, NDUA4, FKBP3, IF4G2, ZYX, CAVN2, SPRE, SF01, CD34, CH10, H2A2B, H2A2C, NQO1, VINC, EI3JB, CLH1, H2A2A, GPSM1, IF4G1, KCRS, LPPRC, AT1A2, CAND2, RS9, CMYA5, FHOD3, ATPMK, MIC27, MSRB2, NP1L4, MTCH1, MTCH2, PICAL, NDUAC, HNRPQ, HUWE1, LC7L2, MIC10, NEXN, SRCA, LNP, CLAP1, SRA1, UBP2L, NRAP, BDH, GLRX5, ATPF1, EFTU, H2A3, LPP, MYPT2, IF4B, ECHM, RCN3, SYIM, EIF2A, ODPX, EEA1, ODP2, ECHA, COQ3, RL24, FLNA, TIDC1, PLIN5, SYP2L, SSDH, THIM, MIC60, PABP2, BOLA3, SYEP, LONM, H2A1F, H2A1H, H2A1K, SEPT8, PGP, AL4A1, SLAI2, PDLI5, PYGB, PAK2, AFG32, EIF3B, FIBB, COXM2, COQ9, SDHA, SIR5, ACD10, NDUS8, NNRE, HIBCH, THIL, MARE2, QCR9, H2AJ, DC1L1, SPART, NAR3, MIC13, CLYBL, PP14C, TXLNB, MAVS, MYH9, VIGLN, PSMD2, AT1A1, LMCD1, HNRPU, S25A3, FLNC, SFPQ, NDUS1, MIC25, ATPG, SH3L3, UBAP2, NDUS2, EIF3H, CISD1, HEMO, EGLN1, L2HDH, RPN1, NDUV1, GRHPR, MYH7, PCCA, UGPA, ETFD, THIKA, TRFE, TOIP1, MACD1, CLIP1, K2C5, UBXN1, ALPK3, RT02, CPT1B, TALDO, ROAA, THTM, STML2, PACN3, ECHB, PLST, ACON, DCTN2, NAMPT, PPIF, NDUAA, ETFA, GRPE1, PARK7, NDUS5, DNJA3, PCCB, MCCA, PPR3A, EH1L1, ACS2L, RRBP1, GDIR1, NDUA5, COX6C, TOM22, ATP5L, NDUB2, COXM1, RM24, NDUC2, DECR, QCR8, NDUA2, FIS1, SDHB, NDUB4, NDUB5, NDUB9, AT5F1, RS21, ACO13, 1433B, CYB5B, KGD4, NDUA6, NDUB3, PSMD9, RL14, NDUB7, M2OM, UCRI, MIC19, OCAD1, PIN4, NDUS4, RT28, SERB1, SPCS2, SSBP, QCR1, NSF1C, C560, CISY, TOM70, RS19, ODPB, HNRPM, PGM1, SCOT1, CY1, HINT2, GAL3A, MCEE, CHCH2, ERP44, NOL3, MMAB, ODO2, COA3, RT33, ATPD, NDUB8, NDUV2, IDH3A, F162A, ARMC1, RL37, QCR7, RL4, EF1G, EFHD2, PRS37, ATPO, QCR2, PGAM1, MYPT1, LNEBL, TELO2, NDUA9, NDUS7, NDUA8, NDUBA, NDUS3, CRIP2, ETFB, ATP5H, MIC26, MMSA, EHD4, NDUAD, POPD1, HRG, PALLD, JPH2, IVD, NHRF2, PALMD, ACTN2, AK1A1, DBLOH, MYOZ2, PDK2, HSPB8, HIG1A, BAG3, AUHM, MACF1, VAPB, NDRG2, ACOT2, QKI, PRS30, UBQL2, H2AY, GLYG, ACOX1, DEST, KAD1, PSA1, KAD2, KAD3, CAD13, PYGM, IF4H, COR1B, SUCA, ECI2, SH3BG, TAGL2, PACN2, EHD1, AIFM1, NDUA7, BAG6, USO1, PLM, LETM1, SUCB2, SUCB1, K2C6B
Species: Mus musculus
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Wu JL, Chiang MF, Hsu PH, Tsai DY, Hung KH, Wang YH, Angata T, Lin KI. O-GlcNAcylation is required for B cell homeostasis and antibody responses. Nature communications 2017 8(1) 29187734
Abstract:
O-linked N-acetylglucosamine (O-GlcNAc) transferase (Ogt) catalyzes O-GlcNAc modification. O-GlcNAcylation is increased after cross-linking of the B-cell receptor (BCR), but the physiological function of this reaction is unknown. Here we show that lack of Ogt in B-cell development not only causes severe defects in the activation of BCR signaling, but also perturbs B-cell homeostasis by enhancing apoptosis of mature B cells, partly as a result of impaired response to B-cell activating factor. O-GlcNAcylation of Lyn at serine 19 is crucial for efficient Lyn activation and Syk interaction in BCR-mediated B-cell activation and expansion. Ogt deficiency in germinal center (GC) B cells also results in enhanced apoptosis of GC B cells and memory B cells in an immune response, consequently causing a reduction of antibody levels. Together, these results demonstrate that B cells rely on O-GlcNAcylation to maintain homeostasis, transduce BCR-mediated activation signals and activate humoral immunity.
O-GlcNAc proteins:
FAIM3, BLTP1, BCORL, M3K15, KANL3, EXC6B, PLHD1, CTTB2, MYO1E, SCLT1, TAF4B, TCOF, FLOT1, OXLA, HDAC1, SYPL1, SEM4D, MA2B1, PPE2, PLD3, DPOD2, NOCT, HNRH1, API5, DFFA, MMP8, DPM1, EIF3D, ESS2, CTNL1, VTI1B, S28A2, FA5, CO4B, IGKC, LAC1, IGHA, IGHDM, HA11, LAMC1, TBA1B, LDHA, HVM51, SPTA1, ZFP1, EGR1, ENPL, RPB1, ITB1, ENV1, 4F2, HS90B, HA2B, HB2A, CD44, BLK, CN37, LAMP2, ZFP37, PTBP1, HB2I, BASI, FAS, EVI2A, MDR1A, BGAL, ITAL, LYN, TLN1, MOES, U2AF2, MAP4, GNA13, RL3, CATG, DPP4, PTN6, HEXA, NKTR, HMGB2, SUH, CEAM1, GTR3, DRG1, RAB5C, CD22, FMR1, VGFR1, GRP75, CAP1, ECI1, FOXK1, STAT1, NKX25, TCPQ, H11, H13, IL12B, CAPZB, RL5, VDR, RET3, ADCY7, VA0D1, AAAT, IMA1, STOM, FUS, NICA, RU2A, EF2, AAAS, RUVB1, ABCE1, DCAF7, 1433G, ACTA, RS6, VATB2, RL23, RL8, PP2BA, RACK1, TBB4B, M4K1, ITPR3, SURF6, ELAV1, EVL, H2B1A, AT8A1, TCPH, TCPB, NXN, TBB5, HNRL2, CREB1, PLAK, 3MG, CO6A1, LG3BP, COE1, CNN2, NSUN2, HMHA1, SNUT2, SMCA4, TPC10, TGRM2, I20L2, LMF1, PUF60, ZSWM8, PRRC1, SC31A, CPZIP, ITAD, ULK4, ITA1, DYHC2, LIN54, JKIP3, GRHL3, MYO1G, SIN3A, IRAG2, SAMH1, KHDR1, LY75, RASA3, NPT2A, CAPR1, ARHG2, PML, IMA5, LAP2B, PRP4B, M4K2, TS101, PLSL, CTNA2, VSX2, CD37, SERA, PCBP2, TIF1B, COCH, NUP62, RALY, UT14A, ARG39, CLH1, ATS16, F120A, NOP58, TEDC2, U520, RRP12, SMHD1, ANO6, TTBK1, CHD4, SARM1, NUP98, RASL2, TNKS1, AT1A2, NFRKB, DDX55, DNA2, H2B1C, CMYA5, GIMA8, CYFP1, SPAG5, HNRPQ, RPF1, MBB1A, PRC2A, ADCY2, MOGS, SDA1, FA98B, WIPI2, TRRAP, XYLT1, WDR82, GNS, ERLN2, S38A9, WASF2, S2512, NIM1, TBL1R, ZN526, CARF, HES7, UNC80, RBGPR, ECHA, ELMO1, ATOSB, KMT2C, FLNA, TPC2, RBBP5, POGZ, DOC10, SYFA, SMKZ, COR2A, RBM14, DOCK2, CASP9, RAE1L, NUP88, RPB2, UACA, SYEP, P66A, VPS50, COPA, VWF, TXTP, ZN536, LMBD1, R4RL1, C2D1A, URP2, STX5, GT251, SDHA, PO121, ABLM1, COL12, ALAT1, RORB, PDLI2, ERO1B, CD177, PSPC1, NUP58, STAB2, LRC8C, COX18, MAVS, PLBL1, UN93B, EVI2B, MYH9, ESIP1, VIGLN, PSMD2, HNRL1, CCAR2, SP7, RECQ5, SFXN3, IF4A3, RINI, DDX1, UBAP2, S15A4, DNJC9, MASP2, UXS1, CSCL1, BMP2K, CYRIB, SYDC, C1TC, GLYR1, PDIA6, CIC, S12A6, ATAD3, MYO5A, MCLN1, ABEC3, STML2, SFXN1, PRP19, TARA, MCRS1, RTCB, NDUS5, S12A9, SF3B1, ANR17, NU155, TR34A, BAP1, PRP8, NUDC2, TSN31, RN138, RTRAF, RU2B, YETS4, M2OM, MIC19, SNX2, DDX28, CXXC1, RUSD4, ILF2, CHTOP, LUC7L, DIM1, MCES, SEC13, SP2, NOP56, U2AF1, EF1G, MCEM1, EVPL, PRP4, CMTR1, WWP2, DHB11, PESC, TLR9, IRX6, KRT81, RBP2, AFF4, KAT2B, STK3, NUP50, DDX21, ACINU, SIGIR, ZN207, SLAF1, SON, H2AY, MTA2, SAE1, MYO1C, RUVB2, TRPV2, PFKAP, ARC1B, ASAH1, VAPA, EHD1, IF2G, CLIC1, HNRPF
Species: Mus musculus
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